High prevalence of DR-TB (drug-resistant tuberculosis): An Indicator of public health negligence

Pak. J. Pharm. Sci., Vol.32, No.4, July 2019, pp.1529-1536 1529
High prevalence of DR-TB (drug-resistant tuberculosis): An Indicator
of public health negligence
Rida Masood, Iyad Naeem Muhammad*, Tuba Siddiqui,
Madiha Mushtaque and Asma Irshad
Department of Pharmaceutics, Faculty of Pharmacy and Pharmaceutical Sciences, University of Karachi, Karachi, Pakistan
Abstract: Tuberculosis (TB) is among the 10 most common worldwide causes of mortality. In Pakistan, estimated
510,000 tuberculosis patients had been diagnosed with an occurrence of 276/100,000. As per most recent global TB
report 2018, Pakistan is amongst the 30 countries high TB with drug-resistant Mycobacterium tuberculosis particularly
MDR (multi-drug resistant strains). A retrospective study had been designed using DR-TB patients’ records from
January 2013 to the December 2017 year from a public sector hospital in Karachi. Overall 315 drug-resistant
tuberculosis patient’s data had been incorporated in the study. All data had been analyzed using SPSS version 16
software. Chi-square test had been used to analyze the data with CI (confidence interval) 95% and level of significance
5%. The study result showed that 64.1% MDR patients, 27.9% MTB rifampicin resistance, 4.8% mono-drug resistant ,
XDR(1.6%), 1% poly-drug resistant and only 0.6% are MDR suspects showing no association of DR-TB with gender (p-
value 0.787), age group (p-value 0.757), treatment outcomes (p-value 0.549), year of registration( p-value 0.206), first
line treatment history(p-value 0.643) with a 95% confidence interval. The drug resistance TB cases have been
periodically rising every year. Early identification is required to reduce the percent mortality and inhibit the disease
transmission.
Keywords: Mycobacterium tuberculosis, drug-resistant tuberculosis (DR-TB), first-line and second-line anti-
tuberculosis treatment.
INTRODUCTION
Tuberculosis (TB) continues to be a worldwide public
health issue of severe extent demanding urgent attention.
Present worldwide efforts to prevent and control
tuberculosis have 3 distinct but coinciding extents:
economic, humanitarian and public health. Worldwide,
TB is among the 10th
utmost common causes of mortality.
(Pakistan Observer, 2017)
DR-TB is a persistent threat. In 2016, there had been
600,000 new cases of RR-TB (Rifampicin resistance
tuberculosis, which is the most effective first-line anti-
tubercular drug) of which 490,000 cases had MDR-TB.
Nearly 47% of drug-resistant tuberculosis cases were in
China, the Russian Federation, and India. (World Health
Organization, 2017b)
Above 2 billion individuals, (equivalent to one-third of
the population of the world) suffer from M. tuberculosis
bacilli. 1 in 10 TB patients progresses to active
tuberculosis. Each year around 1.8 million individuals
demises because of tuberculosis, which equals 4,500
demises/day, a majority of which occur in immensely
populated areas, such as China, Pakistan, Bangladesh,
Indonesia and India where the 48% of new tuberculosis
cases occur. (Dye, 2006). In Pakistan, around 297,000
tuberculosis cases are reported per year. Multidrug-
resistant tuberculosis (MDR-TB) is a type of tuberculosis
categorized by the resistance of two or more effective
first-line anti-tubercular medicine particularly isoniazid
and rifampicin. Internationally, approximately 440,000
MDR-TB cases emerge each year which equals 3.6% of
overall new tuberculosis patients. As per WHO, Pakistan
is among the 27 countries with a huge problem of multi-
drug resistant tuberculosis. MDR-TB occurs in 35% of
formerly treated TB patients and 2%-3.2% of recently
diagnosed (Javaid et al., 2008). Treatment success rates in
MDR-TB are less compared to DS-TB (drug-susceptible
tuberculosis). (Rao et al., 2009), (World Health
Organization, 2010)
A study conducted on 50,000 tuberculosis cases in thirty-
five countries, International Union against Tuberculosis
and Lung Diseases, CDC (Centers for Disease Control
and Prevention), and WHO noticed that in Russia,
Estonia, India, Latvia, Argentina, Ivory Coast, and The
Dominican Republic, M. tuberculosis bacilli were
resistant to the most potent first-line anti-tubercular drugs
i.e. rifampicin and isoniazid. One-third of the countries
investigated had multi-drug resistant tuberculosis level
ranging between 2 to 14%. (World Health Organization,
2000). According to another study (World Health
Organization, 2000) among 64,104 tuberculosis cases
from fifty-eight geographical locations, DR-TB (drug-
resistant tuberculosis) was found between 2.9-40.8%. The
occurrence of DR-TB was directly linked to the
proportion of registered earlier cured cases and inversely*Corresponding author: e-mail: iyanaeem@uok.edu.pk

High prevalence of DR-TB (drug-resistant tuberculosis): An indicator of public health negligence
Pak. J. Pharm. Sci., Vol.32, No.4, July 2019, pp.1529-15361530
linked to the proportion of tuberculosis cases cured under
DOTS.
The development of resistance to anti-tubercular drugs
and mostly MDR-TB is an important public health issue
and a bottle neck like in effective tuberculosis control.
(Toman, 1979) (Grover and Takkar, 2008)
MATERIALS AND METHODS
Research design
A retrospective observational study had been designed
using DR-TB patients’ records from 2013 to 2017 year
from a teaching, tertiary care government hospital in
Karachi.(Goodhand et al., 2012) The entire bioethics
requirement has been approved from Bioethical
Institutional Review Board Committee (IRB) of hospital.
Setting
New and direct observed therapy, short course DOTS
treated patients having DR-TB via established regimen by
world health organization. The treatment regimen was
decided on the individual basis subject to clinical
conditions. A drug-resistant tuberculosis patient offers
MTB-rifampicin drug resistance, MDR, mono drug
resistance, XDR and poly-drug resistance.
Mono-resistance-TB
Tuberculosis in which M. tuberculosis offers resistance to
only one first-line anti-tubercular drug.
Poly-resistance-TB
Mycobacterium carries resistance to more than one first-
line anti-tubercular drug, excluding isoniazid and
rifampicin both.
Multidrug resistance (MDR)
Mycobacterium tuberculosis which carries resistance to
most effective first-line anti-tubercular drugs i.e.
rifampicin and isoniazid.
Extensive drug resistance (XDR)
A very uncommon type of MDR-TB in which
Mycobacterium tuberculosis bacteria offers resistance to
isoniazid and rifampicin but also to any fluoroquinolone
and one of three second-line anti-tubercular injectable
drugs i.e. capreomycin, kanamycin and amikacin.
TB- Rifampicin resistance (RR)
Resistance to rifampicin is identified via phenotype and
genotype methods. Rifampicin resistance might be with or
without the resistance other anti-tubercular drugs.
Rifampicin resistance resides presents either in MDR-TB,
XDR-TB, mono-resistance tuberculosis and poly-
resistance tuberculosis. (World Health Organization,
2017a)
Population
The population comprised of all drug-resistant
tuberculosis patients from a government hospital from the
period of January 2013 to December 2017 in Karachi
Inclusion criteria
 New and direct observed therapy treatment, short course
(DOTS) treated cases of DR-TB
 No restriction of age limit
Exclusion criteria
 Drug-susceptible tuberculosis
Collection of data
Overall, 315 drug-resistant tuberculosis patients’ data had
been included in the study. Patient treatment cards,
together with TB register had been reviewed so as to
record patient characteristics along with treatment
outcomes. Through standard definitions, a record was
prepared for the TB category and final treatment result.
Death has been explained because of any reason while
treatment continued with anti-tuberculosis drugs.
Following data had been collected
1. Patient age and gender
2. Year of registration of patient in the hospital
3. Treatment outcomes
4. Type of DR-TB
5. First line Tuberculosis drug treatment history and
outcomes
6. Second line tuberculosis drug treatment history and
outcomes
7. Site of DR-TB
8. DST (drug-susceptibility testing of first-line and
second-line anti-tubercular drugs)
STATISTICAL ANALYSIS
An explanatory and methodical approach was followed to
investigate the clinical administration and outcomes. The
data was assessed via SPSS v16 software which was
subsequently sorted to get the appropriate frequencies,
statistics, cross tables, bar graph/diagram plotted etc. (for
more understanding). Chi-square test utilized to evaluate
the data with 95% CI (confidence interval) and 5% level
of significance.
RESULT
Fig. 1: History of previous first-line drug therapy given to
DR-TB patients.

Rida Masood et al
DISCUSSION
DR-TB is one of the constantly puzzling hazards. In 2016,
600,000 new cases of RR-TB (rifampicin resistance
tuberculosis) were registered which (rifampicin) is an
efficient first-line anti-tubercular drugs. Out of 600,000
new cases 490,000 had multi-drug resistant tuberculosis.
Almost half of the drug-resistant tuberculosis cases i.e.
47% were observed in the Russian Federation, India, and
China. (World Health Organization, 2017b)
Globally in 2016, an estimated 19% (9.8-27%,
Confidence Interval: 95%) of formerly treated cases and
4.1% (CI: 95% [conﬁdence interval] 2.8-5.3%) new cases
had drug-resistant tuberculosis (MDR/RR-TB). (World
Health Organization, 2017b).
Around thirty-five countries have introduced short
treatment regimens for RR-TB or MDR-TB. Efforts to
upsurge therapeutic outcomes for extensive and multi-
drug resistant tuberculosis, eighty-nine countries had
begun utilizing bedaquiline however delamanid was
Table 1: Year-wise registration of Type of DR-TB patient
Year of registration
Total
2013 2014 2015 2016 2017
Type of DR-TB
MDR 11 40 55 54 42 202
MTB Rifampicin Resistance 2 14 28 12 32 88
Mono drug resistance 0 1 3 4 7 15
XDR 0 1 1 2 1 5
Poly drug resistance 0 0 1 2 0 3
MDR suspects 0 1 0 0 1 2
Total 13 57 88 74 83 315
Table 2: Age-wise distribution of DR-TB patients
Age Group
Total5-14
yrs
15-24
yrs
25-34
yrs
35-44
yrs
45-54
yrs
55-64
yrs
65+
yrs
2013
Type of
DR-TB
MDR 2 4 2 2 0 1 11
MTB rifampicin resistance 1 0 0 0 1 0 2
Total 3 4 2 2 1 1 13
2014
Type of
DR-TB
MDR 3 12 12 7 4 2 0 40
MTB rifampicin resistance 1 3 2 2 1 4 1 14
Mono drug resistance 0 1 0 0 0 0 0 1
XDR 0 0 1 0 0 0 0 1
MDR suspects 0 0 0 1 0 0 0 1
Total 4 16 15 10 5 6 1 57
2015
Type of
DR-TB
MDR 3 23 10 6 4 4 5 55
XDR 0 0 1 0 0 0 0 1
Poly drug resistance 0 1 0 0 0 0 0 1
Total 3 38 17 10 6 8 6 88
2016
Type of
DR-TB
MDR 3 21 12 9 4 5 0 54
XDR 0 0 0 0 0 1 1 2
Total 5 29 15 11 4 8 2 74
2017
Type of
DR-TB
MDR 0 14 12 9 4 2 1 42
XDR 0 1 0 0 0 0 0 1
MDR suspects 0 1 0 0 0 0 0 1
Total 2 27 16 18 12 4 4 83

prescribed by fifty-four countries from June 2017. (World
Health Organization, 2017b).
Fig. 2: Site of DR-TB of DR-TB patients
In current study, number of drug-resistance tuberculosis
patients has been increase every year as shown in table 1,
and most commonly occurred in 15-44 years age group as
shown in table 2.The rate of successful management for
MDR-TB can be ≈ 70-90% (Sampathkumar, 2008).
Approximately, sixty percent mortality rate has been
witnessed among MDR-TB (Irfan et al., 2006) in contrast,
the low percent mortality was found in HIV infections
(Seung et al., 2009). A study by Khurram et al., in 2011
observed the 10% cure rate in MDR-TB patients while
40% had died, defaulted and treatment failure were 30%
and 20% respectively (Khurram et al., 2011) In all,
present study found the cure rate of (110/315, 34.9%)
among multi-drug resistant-TB, however, 42/315
(13.3%) patients were died and 10/315 (3.2%) were
treatment failed. Moreover, 15 (4.8%) patients were non-
complaint, 9 (2.9%) patients had completed their
treatment, 30 (9.5%) patient had failed to evaluate as well
as 99 (31.4%) patients had still undergone treatment from
2013 till 2017 as shown in table 5. An investigation
conducted in Pakistan, found the resistance among
isolates of MDR-TB i.e. 80% against pyrazinamide and
streptomycin and 66% against ethambutol. However,
some researchers observed increasing resistance towards
quinolones (ciprofloxacin and ofloxacin) due to excessive
and inappropriate usage of these quinolones. (Khurram et
al., 2011). Another study identified resistance towards
ethambutol and pyrazinamide to be 17.61% and 10.79%,
respectively. However, the drug sensitivity data for 2nd-
line antibiotics were not available in MDR-TB patients
(Saeed et al., 2009). Another research in 2006,
documented the presence of 38% cases of MDR-TB that
were found resistant to 6 Ist-line anti-tuberculous agents,
20%, 25% and 12% cases showed resistance toward 5, 4
and 3 first-line anti-tuberculosis agents respectively.
Nevertheless, the 2nd-line antibiotics sensitivity data were
also not recorded in the work (Javaid and Ziaullah, 2006).
The current investigation reported, 36 (11.4%) to be
resistant to HRZE, 76 (24.1%) resistant to HR, 29 (9.2%)
resistant to HRZES, 10 (3.2%) resistant to HRZS, 12
(3.8%) resistant to HRS, 10 (3.2%) resistant to HRE, 26
(8.3%) resistant to HRZ, 106 (33.7%) resistant to R, 5
(1.6%) resistant to HRES, 1 (0.3%) resistant to H and 1
(0.3%) resistant to R respectively (table 6).
The current investigation reported, resistance profile to
2nd-line anti-tuberculous agents were 13 (4.1%) to FQ
and Eto, 1 (0.3%) resistance to Am and Km, 24 (7.6%)
resistant to Eto, 64 (20.3%) resistance to FQ, 2 (0.6%)
resistance to Km, Cm, Am and Ofx, 1 (0.3%) resistance to
Am, Cm, Km, Ofx and Lzd, 1 (0.3%) Km, Am and Ofx, 2
(0.6%) Am, Cm. Furthermore, upto 207 (65.4%) showed
no resistance to second-line drugs as shown in table 7.
Kruk et al., (2008) had reported 6-30% default cases
(Kruk et al., 2008). The causes of drug intolerance to 2nd-
line treatment include: clinical failure of rapid
improvement and increasing expenses of diagnostic test
and treatment. However, the expenses incurred on current
study i.e. diagnostics/treatment were funded by
governmental/ non-governmental organizations.
Nevertheless, the non-respondents of MDR-TB have
severe consequences. Additionally, the disease
progression may cause serious complications that may
even lead to patient’s death. Furthermore, these non-
respondents may help in the spread of disease. The
current research most frequently observed DR-TB during
the age of 15-24 years (table 2). Male DR-TB patients
contributed 133/315 as shown in table 3.
More than 50% of DR-TB patients hailed from low socio-
economic, illiteracy, and over-populated groups. A
previous study revealed 95% of patients were treated for
TB earlier and incomplete tubercular therapy compliance
whereby 65.5% patients. (Khurram, 2009). In contrast, the
present work determined 25.4% DR-TB patients who
were not previously treated with any ATT while rest 74.6
% were treated with ATT previously. Among them,
59.7% and 7.9% had previously been treated with CAT I
and II respectively. Furthermore, CAT I therapy was
repeated in 3.5% of patients, defaulters were 1.3% and
only 2.2% had completed the treatment course as shown
in fig. 1.
Upto 92% of DR-TB patients were not treated with any
2nd line agent previously; in-contrast only 7.9% patients
had been treated with second-line drugs (table 4). The
treatment cost of patients of the MDR-TB patient in the
advanced world is approx. £60,000 which is around
10663685.36 Pakistani Rupees or US $100,000 (Zumla
and Grange, 2001); hence, management of patients
(priorities etc.) of DR-TB at government hospitals is
enormously challenging in resource-limited situations. In
order to control and prevent the spread and development
of MDR-TB, one should focus on effective treatment of
drug-susceptible tuberculosis. (Khurram et al., 2011).

Rida Masood et al
Table 3: Gender wise distribution of DR-TB patients
Gender Of Patients
Total
Male Female
2013
Type of DR-TB
MDR 5 6 11
MTB rifampicin resistance 0 2 2
Total 5 8 13
2014
Type of DR-TB
MDR 18 22 40
Mono drug resistance 0 1 1
XDR 0 1 1
MDR suspects 0 1 1
Total 22 35 57
2015
Type of DR-TB
MDR 20 35 55
XDR 0 1 1
Poly drug resistance 0 1 1
Total 29 59 88
2016
Type of DR-TB
MDR 23 31 54
XDR 2 0 2
Total 33 41 74
2017
Type of DR-TB
MDR 19 23 42
XDR 0 1 1
MDR suspects 0 1 1
Total 44 39 83
Table 4: Previous second-line treatment history administered to DR-TB patients
Previously received SLD
Total
No Yes
Type of DR-TB
MDR 184 18 202
XDR 4 1 5
MDR suspects 0 2 2
Total 290 25 315
Table 5: Treatment outcome of DR-TB patients
Treatment outcome
Total
Cured Died Failed
Non-
compliant
Completed
Not
evaluated
Still under
Treatment
Type of
DR-TB
MDR 73 28 8 8 8 20 57 202
MTB rifampicin
resistance
33 12 1 5 1 7 29 88
Mono drug
resistance
3 0 0 1 0 2 9 15
XDR 0 1 1 1 0 1 1 5
MDR suspects 0 1 0 0 0 0 1 2
Total 110 42 10 15 9 30 99 315

This study recorded 64.1 % MDR patients, 27.9% MTB
rifampicin resistant, 4.8% mono-drug resistant, XDR
(1.6%), 1% poly-drug resistant and only 0.6% are MDR
suspects as shown in fig. 3. Out of 315 patients, 195
patients suffering from pulmonary multi-drug resistant
tuberculosis whereas only 4 patients suffering from extra
pulmonary multi-drug resistant tuberculosis, 84 patients
were diagnosed with rifampicin resistance pulmonary
tuberculosis and 4 patients with rifampicin resistance
extra-pulmonary tuberculosis, 15 patients showed Mono
drug resistant pulmonary tuberculosis, 4 patients were
XDR pulmonary tuberculosis, 3 patients showed poly
drug resistant tuberculosis whereas only 1 patient showed
XDR extra-pulmonary tuberculosis and 1 patients showed
extra-pulmonary MDR suspects as shown in fig. 2. An
earlier work reported a high incidence of XDR-TB in
Pakistan thereby expressing serious concerns inspite of
the fact that a study in 2009, reported 4.5% rate of XDR
among MDR-TB that is within the global average of
6.6%-23.7%. (Wright et al., 2009) (Hasan et al., 2010).
In 2008, ≈3-5 lac MDR-TB cases reported around the
globe. Amongst all, 3.6% [95% CI (confidence interval):
3.0-4.4] were identified as multi-drug resistant
Table 6: Drug susceptibility testing of first-line anti-tubercular drugs
Total
2013 2014 2015 2016 2017
Resistance to first-line
drugs
MDR suspect 0 1 0 0 1 2
HRZE 1 8 9 14 4 36
HR 1 6 18 25 26 76
HRZES 4 12 7 3 3 29
HRZS 2 1 5 1 1 10
HRS 2 4 5 1 0 12
HRE 1 2 2 1 4 10
HRZ 0 4 6 11 5 26
R 2 16 32 17 39 106
HRES 0 3 2 0 0 5
H 0 0 1 0 0 1
RS 0 0 1 0 0 1
RZ 0 0 0 1 0 1
Total 13 57 88 74 83 315
Where H= Isoniazid; R= Rifampicin; Z= Pyrazinamide; E= Ethambutol; S= Streptomycin
Table 7: Drug susceptibility testing of second-line anti-tubercular drugs
Total
2013 2014 2015 2016 2017
Resistance to
second-line drugs
No resistance 8 38 56 41 64 207
FQ, Eto 0 0 7 4 2 13
KM, Am 1 0 0 0 0 1
Eto 0 4 6 10 4 24
FQ 4 14 18 16 12 64
Km, Cm, Am, Ofx 0 1 0 0 1 2
Am, Cm, Km, Ofx, Lzd 0 0 1 0 0 1
Km, Am, Ofx 0 0 0 1 0 1
Am, Cm 0 0 0 2 0 2
Total 13 57 88 74 83 315
Where FQ= Fluoroquinolones; Eto= Ethionamide; Km= Kanamycin; Am= Amikacin; Cm= Capreomycin; Ofx= Ofloxacin; Lzd=
linezolid
Table 8: Chi square test for association
Association of DR-TB with Chi-square p-value CI α-value Remarks
Gender 2.433 0.787 95% 0.05 No
Age group 24.388 0.757 95% 0.05 No
Treatment outcome 28.407 0.549 95% 0.05 No
Year of registration 24.881 0.206 95% 0.05 No
FLD-treatment history 21.875 0.643 95% 0.05 No
SLD treatment history 30.868 0.000 95% 0.05 Yes
Site of DR-TB 22.564 0.012 95% 0.05 Yes
Treatment outcome 28.407 0.549 95% 0.05 No

Rida Masood et al
tuberculosis. However, nearly 50% of multi-drug resistant
tuberculosis cases were recorded in India and China.
WHO report in 2010 stated 150,000 deaths among MDR
tuberculosis patients. Moreover, 27 countries including
Pakistan were reported with a high burden of multi-drug
resistance as well as annual incidence of MDR-TB was
4000 and at least 10% new cases were registered as
MDR-TB (World Health Organization, 2010). The
therapy of MDR-TB has involves expenses (50 to 200
times) than DS-TB. In all, the cost of therapy is 10 times
greater than DS-TB.
Fig. 3: Type of DR-TB patients
Approximately 5 lac cases of MDR-TB are reported each
year globally, while 9% of MDR-TB was actually XDR
(extensively drug-resistant) isolates of Mycobacterium.
Unfortunately, prolonged treatment, toxicity, high
expenses of therapy of DR-TB and low rate of success
(i.e. <20%) were the major reasons for XDR
Mycobacterium strains. (D'Ambrosio et al., 2015)
TB is one of the main health issues emerging around the
globe, one third population are infected with tubercle
bacilli and 1/sec is the rate of new infection. In India,
new cases of MDR-TB were 2-3%, however, 12-17%
were relapsed cases. The most important cause of MDR-
TB might be non-adherence of patients towards anti-
tuberculous therapy due to ADR. (Sood et al., 2016). The
recent enhancement in DR-TB cases and the shortage of
ATT agents is alarming for the future control of TB. The
frequent emergence of DR-TB is mainly due to the
utilization of one or more anti-tuberculous agents to sub-
therapeutic levels. (Muttil et al., 2009).
Early identification is required to reduce the mortality
percentage and to inhibit the disease transmission.
(Boehme et al., 2010). In Pakistan, the cases of DR-TB
have occurred more increasingly, however, very few
cases are reported because of limited access to culture
and sensitivity facilities around the country and many
more pertinent factors.
The drug resistant TB cases have been periodically rising
every year. On-going surveillance programs as well as
efficient implementation of National TB Control Program
(NTP) using direct observed therapy, short course
procedure are essential in order to minimize the incidence
of DR-TB. The preventive measure includes quick and
accurate detection of TB cases and their effective
management. An inappropriate control program may
results to MDR-tuberculosis much faster when treated
improperly. The direct observed therapy, short courses
(DOTS) policy should be employed to prevent the
emergence of resistant organisms and proper utilization of
2nd
line agents for the management of MDR-TB is the
major step for the effective control and prevention of
MDR-TB. (Javaid et al., 2008)
CONCLUSIONS
Early identification is warranted to reduce the mortality
percentage and to inhibit the disease transmission. On-
going surveillance program as well as efficient
implementation of National TB Control Program (NTP)
Pakistan using DOTs procedure is essential in order to
minimize the incidence of DR-TB.
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High prevalence of DR-TB (drug-resistant tuberculosis): An Indicator of public health negligence

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